Transient Receptor Potential Vanilloid 4-Induced Modulation of Voltage-Gated Sodium Channels in Hippocampal Neurons

详细信息    查看全文

• 作者：Zhiwen Hong ; Pinghui Jie ; Yujing Tian ; Tingting Chen ; Lei Chen…
• 关键词：Transient receptor potential vanilloid 4 ; Voltage ; gated sodium channels ; TTX ; sensitive sodium channel ; Intracellular signaling pathway ; α ; subunit of sodium channel
• 刊名：Molecular Neurobiology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：53
• 期：1
• 页码：759-768
• 全文大小：634 KB
• 参考文献：1.Nilius B, Szallasi A (2014) Transient receptor potential channels as drug targets: from the science of basic research to the art of medicine. Pharmacol Rev 66(3):676–814CrossRef PubMed
  2.Vincent F, Duncton MA (2011) TRPV4 agonists and antagonists. Curr Top Med Chem 11(17):2216–2226CrossRef PubMed
  3.Nilius B, Voets T (2013) The puzzle of TRPV4 channelopathies. EMBO Rep 14(2):152–163CrossRef PubMed PubMedCentral
  4.Grant AD, Cottrell GS, Amadesi S, Trevisani M, Nicoletti P, Materazzi S, Altier C, Cenac N, Zamponi GW, Bautista-Cruz F, Lopez CB, Joseph EK, Levine JD, Liedtke W, Vanner S, Vergnolle N, Geppetti P, Bunnett NW (2007) Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 578(Pt 3):715–733CrossRef PubMed PubMedCentral
  5.Egbuniwe O, Grover S, Duggal AK, Mavroudis A, Yazdi M, Renton T, Di Silvio L, Grant AD (2014) TRPA1 and TRPV4 activation in human odontoblasts stimulates ATP release. J Dent Res 93(9):911–917CrossRef PubMed PubMedCentral
  6.Ryskamp DA, Witkovsky P, Barabas P, Huang W, Koehler C, Akimov NP, Lee SH, Chauhan S, Xing W, Rentería RC, Liedtke W, Krizaj D (2011) The polymodal ion channel transient receptor potential vanilloid 4 modulates calcium flux, spiking rate, and apoptosis of mouse retinal ganglion cells. J Neurosci 31(19):7089–7101CrossRef PubMed PubMedCentral
  7.Chen L, Liu C, Liu L (2009) Osmolality-induced tuning of action potentials in trigeminal ganglion neurons. Neurosci Lett 452(1):79–83CrossRef PubMed PubMedCentral
  8.Shibasaki K, Suzuki M, Mizuno A, Tominaga M (2007) Effects of body temperature on neural activity in the hippocampus: regulation of resting membrane potentials by transient receptor potential vanilloid 4. J Neurosci 27(7):1566–1575CrossRef PubMed
  9.Li L, Yin J, Jie PH, Lu ZH, Zhou LB, Chen L, Chen L (2013) Transient receptor potential vanilloid 4 mediates hypotonicity-induced enhancement of synaptic transmission in hippocampal slices. CNS Neurosci Ther 19(11):854–862CrossRef PubMed
  10.Yu FH, Catterall WA (2003) Overview of the voltage-gated sodium channel family. Genome Biol 4(3):207CrossRef PubMed PubMedCentral
  11.Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltagegated sodium channels. Neuron 26(1):13–25CrossRef PubMed
  12.Scheuer T (2011) Regulation of sodium channel activity by phosphorylation. Semin Cell Dev Biol 22(2):160–165CrossRef PubMed PubMedCentral
  13.Gasser A, Cheng X, Gilmore ES, Tyrrell L, Waxman SG, Dib-Hajj SD (2010) Two Nedd4-binding motifs underlie modulation of sodium channel Nav1.6 by p38 MAPK. J Biol Chem 285(34):26149–26161CrossRef PubMed PubMedCentral
  14.Wittmack EK, Rush AM, Hudmon A, Waxman SG, Dib-Hajj SD (2005) Voltage-gated sodium channel Nav1.6 is modulated by p38 mitogen-activated protein kinase. J Neurosci 25(28):6621–6630CrossRef PubMed
  15.Chen L, Liu C, Liu L, Cao X (2009) Changes in osmolality modulate voltage-gated sodium channels in trigeminal ganglion neurons. Neurosci Res 64:199–207CrossRef PubMed PubMedCentral
  16.Lin L, Liu C, Chen L, Chen L (2011) Hypotonicity modulates tetrodotoxin-sensitive sodium current in trigeminal ganglion neurons. Mol Pain 7:27–32CrossRef
  17.Chen L, Liu C, Liu L (2008) The modulation of voltage-gated potassium channels by anisotonicity in trigeminal ganglion neurons. Neuroscience 154:482–495CrossRef PubMed PubMedCentral
  18.Chen L, Liu C, Liu L (2008) Changes in osmolality modulate voltage-gated calcium channels in trigeminal ganglion neurons. Brain Res 1208:56–66CrossRef PubMed PubMedCentral
  19.Liu L, Chen L, Liedtke W, Simon SA (2007) Changes in osmolality sensitize the response to capsaicin in trigeminal sensory neurons. J Neurophysiol 97:2001–2015CrossRef PubMed
  20.Li L, Qu W, Zhou L, Lu Z, Jie P, Chen L, Chen L (2013) Activation of transient receptor potential vanilloid 4 increases NMDA-activated current in hippocampal pyramidal neurons. Front Cell Neurosci 7:17–26PubMed PubMedCentral
  21.Cantrell AR, Smith RD, Goldin AL, Scheuer T, Catterall WA (1997) Dopaminergic modulation of sodium current in hippocampal neurons via cAMP-dependent phosphorylation of specific sites in the sodium channel αsubunit. J Neurosci 17:7330–7338PubMed
  22.Cantrell AR, Ma JY, Scheuer T, Catterall WA (1996) Muscarinic modulation of sodium current by activation of protein kinase C in rat hippocampal neurons. Neuron 16:1019–1026CrossRef PubMed
  23.Lidtke W, Tobin DM, Bargmann CI, Friedman JM (2003) Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorbditis elegans. Proc Natl Acad Sci U S A 100(Suppl 2):14531–14536CrossRef
  24.Borodinsky LN, Spitzer NC (2006) Second messenger pas de deux: the coordinated dance between calcium and cAMP. Sci STKE (336):pe22
  25.Fridlyand LE, Harbeck MC, Roe MW, Philipson LH (2007) Regulation of cAMP dynamics by Ca2+ and G protein-coupled receptors in the pancreatic beta-cell: a computational approach. Am J Physiol Cell Physiol 293(6):C1924–C1933CrossRef PubMed
  26.Willoughby D, Cooper DM (2006) Ca2+ stimulation of adenylyl cyclase generates dynamic oscillations in cyclic AMP. J Cell Sci 119(Pt 5):828–836CrossRef PubMed
  27.Landa LR Jr, Harbeck M, Kaihara K, Chepurny O, Kitiphongspattana K, Graf O, Nikolaev VO, Lohse MJ, Holz GG, Roe MW (2005) Interplay of Ca2+ and cAMP signaling in the insulin-secreting MIN6 beta-cell line. J Biol Chem 280(35):31294–31302CrossRef PubMed PubMedCentral
  28.Seale AP, Watanabe S, Grau EG (2012) Osmoreception: perspectives on signal transduction and environmental modulation. Gen Comp Endocrinol 176(3):354–360CrossRef PubMed
  29.Liu L, Oortgiesen M, Li L, Simon SA (2001) Capsaicin inhibits activation of voltage-gated sodium currents in capsaicin-sensitive trigeminal ganglion neurons. J Neurophysiol 85(2):745–758PubMed
  30.Onizuka S, Yonaha T, Tamura R, Hosokawa N, Kawasaki Y, Kashiwada M, Shirasaka T, Tsuneyoshi I (2011) Capsaicin indirectly suppresses voltage-gated Na+ currents through TRPV1 in rat dorsal root ganglion neurons. Anesth Analg 112(3):703–709
  31.Chen WN, Lee CH, Lin SH, Wong CW, Sun WH, Wood JN, Chen CC (2014) Roles of ASIC3, TRPV1, and NAv1.8 in the transition from acute to chronic pain in a mouse model of fibromyalgia. Mol Pain 10:40–54CrossRef PubMed PubMedCentral
  32.Lisman JE (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20(1):38–43CrossRef PubMed
  33.Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8(6):451–465CrossRef PubMed
  34.Johnston D, Hoffman DA, Colbert CM, Magee JC (1999) Regulation of back-propagating action potentials in hippocampal neurons. Curr Opin Neurobiol 9(3):288–292CrossRef PubMed
  35.Johnston J, Forsythe ID, Kopp-Scheinpflug C (2010) Going native: voltage-gated potassium channels controlling neuronal excitability. J Physiol 588(Pt 17):3187–3200CrossRef PubMed PubMedCentral
  36.Vacher H, Mohapatra DP, Trimmer JS (2008) Localization and targeting of voltage-dependent ion channels in mammalian central neurons. Physiol Rev 88(4):1407–1447CrossRef PubMed PubMedCentral
  37.Jensen MS, Azouz R, Yaari Y (1996) Spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol 492(Pt 1):199–210CrossRef PubMed PubMedCentral
  38.Magee JC, Carruth M (1999) Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J Neurophysiol 82(4):1895–1901PubMed
  39.Azouz R, Jensen MS, Yaari Y (1996) Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol 492(Pt1):211–223CrossRef PubMed PubMedCentral
  40.Yue C, Yaari Y (2004) KCNQ/M channels control spike afterdepolarization in hippocampal neurons. J Neurosci 24(19):4614–4624CrossRef PubMed
  41.Cao DS, Yu SQ, Premkumar LS (2009) Modulation of transient receptor potential vanilloid 4-mediated membrane currents and synaptic transmission by protein kinase C. Mol Pain 5:5–17CrossRef PubMed PubMedCentral
  42.Hunt RF, Hortopan GA, Gillespie A, Baraban SC (2012) A novel zebrafish model of hyperthermia-induced seizures reveals a role for TRPV4 channels and NMDA-type glutamate receptors. Exp Neurol 237(1):199–206CrossRef PubMed PubMedCentral
  
• 作者单位：Zhiwen Hong (1)
  Pinghui Jie (1)
  Yujing Tian (1)
  Tingting Chen (1)
  Lei Chen (1)
  Ling Chen (1)
  
  1. Department of Physiology, Nanjing Medical University, No. 140, Hanzhong Road, Nanjing, 210029, People’s Republic of China
  
• 刊物主题：Neurosciences; Neurobiology; Cell Biology; Neurology;
• 出版者：Springer US
• ISSN：1559-1182

文摘

Transient receptor potential vanilloid 4 (TRPV4) is reported to control the resting membrane potential and increase excitability in many types of cells. Voltage-gated sodium channels (VGSCs) play an important role in initiating action potentials in neurons. However, whether VGSCs can be modulated by the activation of TRPV4 in hippocampal pyramidal neurons remains unknown. In this study, we tested the effect of TRPV4 agonists (GSK1016790A and 4α-PDD) on voltage-gated sodium current (I _Na) in hippocampal CA1 pyramidal neurons and the protein levels of α/β-subunit of VGSCs in the hippocampus of mice subjected to intracerebroventricular (icv.) injection of GSK1016790A (GSK-injected mice). Herein, we report that I _Na was inhibited by acute application of GSK1016790A or 4α-PDD. In the presence of TRPV4 agonists, the voltage-dependent inactivation curve shifted to the hyperpolarization, whereas the voltage-dependent activation curve remained unchanged. The TRPV4 agonist-induced inhibition of I _Na was blocked by the TRPV4 antagonist or tetrodotoxin. Moreover, blocking protein kinase A (PKA) markedly attenuated the GSK1016790A-induced inhibition of I _Na, whereas antagonism of protein kinase C or p38 mitogen-activated protein kinase did not change GSK1016790A action. Finally, the protein levels of Nav1.1, Nav1.2, and Nav1.6 in the hippocampus increased in GSK-injected mice, whereas those of Nav1.3 and Navβ1 remained nearly unchanged. We conclude that I _Na is inhibited by the acute activation of TRPV4 through PKA signaling pathway in hippocampal pyramidal neurons, but protein expression of α-subunit of VGSCs is increased by sustained TRPV4 activation, which may compensate for the acute inhibition of I _Na and provide a possibility for hyper-excitability upon sustained TRPV4 activation.